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Evolution of DevelopmentEhab Abouheif, Duke University, Durham, North Carolina, USA

Gregory A Wray, Duke University, Durham, North Carolina, USA

The field of evolutionary developmental biology provides a framework with which toelucidate the black box that exists between evolution of the genotype and phenotype by

focusing the attention of researchers on the way in which genes and developmental

processes evolve to give rise to morphological diversity.

Introduction

At theend of the nineteenthand beginning of the twentiethcentury, the fields of evolutionary and developmentalbiology were inseparable. Evolutionary biologists usedcomparative embryology to reconstruct ancestors andphyletic relationships, and embryologists in turn usedevolutionary history to explain many of the processesobserved during animal development. This close relation-ship ended after the rise of experimental embryology andMendelian genetics at the beginning of the twentiethcentury. Now, after almost 100 years of separation, thesetwo fields have reunited to form a distinct discipline calledevolutionary developmental biology, whose aim is tounderstand the relationship between evolution of genotypeand evolution of phenotype, as well as how developmentalgenes and processes evolve.

Embryos and Evolution, HeterochronyRecapitulation, the idea that ancestral adult forms repeatthemselves during the embryonic or juvenile stages of theirdescendants, has been a deeply influential idea in thehistory of biological thought. During the nineteenthcentury, it provided a general framework for reconstruct-ing the ancestors and evolutionary histories for countlessorganisms. The appearance of gill arches during an earlyontogenetic stage of a mammalian embryo, for example,was used as evidence that fish are the ancestors ofmammals.

Ernst Haeckel was perhaps the most influential propo-

nent of recapitulation. In 1874, he put forth his famousbiogenetic law, which states that ontogeny recapitulatesphylogeny. Haeckel used his law to postulate the twenty-two ancestors that appear during the development ofhuman embryos. Although Haeckels primary interest wasin the reconstruction of ancestors and evolutionaryhistories, he wanted to provide a mechanical cause for hisbiogenetic law. This led him to propose that phylogenyliterally causes ontogeny through two processes: terminaladdition, which adds new features to the end of ontogeny,

and condensation, which deletes earlier ontogenetic stageto make room for new features (Gould, 1977).

As the field of comparative embryology blossomeduring the early twentieth century, a considerable body oevidence accumulated that was in conflict with thpredictions of the biogenetic law. Because ontogeny coulonly change by pushing old features backwards i

development (condensation) in order to make room fonew features (terminal addition), the timing of developmental events could only be accelerated. Walter Garstanshowed that this apparent constraint on evolutionarchange in development imposed by the biogenetic law wabroken by numerous organisms: not only can evolutionarshifts in the timing of developmental events occur in thopposite direction (i.e. retardation), but novel features arnot always terminal additions. Garstang wrote a series oinfluential articles and witty poems highlighting thpresence of juvenile features of ancestors in the adustages of descendants. Perhaps the most famous examploccurs in the axolotl, Ambystoma mexicanum (Figure 1

This salamander does not metamorphose, and aquatlarval features, such as gills and a tail fin, are retainethroughout adult life. Conversely, most of the othesalamander species within the same genus undergcomplete metamorphosis and lose their gills and tail fin

Article Contents

Secondary article

. Introduction

. Embryos and Evolution, Heterochrony

. HoxGenes

. Embryology, Palaeontology, Genes and Limbs

Figure 1 The Mexican Axolotl. From Dumeril A (1867) Annales DesSciences Naturelles-Zoologie et Biologie Animale7: 229254.

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Thus, the most parsimonious interpretation of thisobservation is that the ancestral salamanders of thisgenus underwent complete metamorphosis and losttheir gills and tail fin, whereas the retardation ofdevelopment observed in Ambystoma mexicanum is anevolutionarily derived feature relative to its ancestors(Raff, 1996).

Haeckel was aware of exceptions to his biogenetic law,and coined the term heterochrony to describe them.Heterochrony, the dissociation of the relative timing oronset of developmental events between ancestral anddescendent ontogenies, was soon recognized as more therule than the exception. The biogenetic law, and thus anyrelationship between evolutionary and developmentalbiology, began to lose favour. With the contemporaneousrise of Mendelian genetics and experimental embryology,the fields of evolutionary and developmental biology wereset on independent trajectories for most of the twentiethcentury (Gould, 1977; Raff, 1996).

During the last three decades, heterochrony has enjoyed

renewed interest as an important index of evolutionarychange. Although heterochrony provides an adequatedescription of the dissociations possible in the timing oronset of development events between ancestral anddescendent ontogenies, it fails to provide an adequatemechanistic explanation for these developmental events. Ifheterochrony is to remain an informative means to studythe connection between evolution and development, futureresearchmust incorporate recent advances fromthe field ofdevelopmental genetics in order to elucidate the genes andmechanisms that underlie heterochronic changes in evolu-tion (Raff, 1996).

HoxGenes

While evolutionary biologists were renewing their interestin heterochrony, developmental geneticists were discover-ing the existence of sets of genes, specifically transcriptionfactorsand signallingmolecules, whichregulate embryonicdevelopment. The initial characterization of these devel-opmental regulatory genes in the fruitfly, Drosophilamelanogaster (Lewis, 1978; Nu sslein-Volhard andWeischaus, 1980), prompted a search for their counter-parts in other animals. It was soon clear that most

developmental regulatory genes are evolutionarily con-served across a broad range of animal phyla (McGinniset al., 1984).

Perhaps no other class or family of developmentalregulatory genes has sparked the imagination of biologistsas much as the homeotic, or Hox, genes. Hox genesencode transcription factors that control the identity orfate of different regions along the anteroposterior axis ofthe embryo. These genes are generally clustered within thegenome, and in many animals are expressed in the same

relative order along the main body axis as they arpositioned along the chromosome.

Changes in the expression of Hox genes along thanteroposterior axis can lead to changes in the identity obody regions. In one of the most famous examples of homeotic transformation, E. B. Lewis (1978) demonstrated that mutations in the non-protein-coding region i

one of the Hox genes, Ultrabithorax, switch the identity ofate of the third thoracic segment in Drosophila into thsecond. The third thoracic segment possesses a pair osmall balancing organs called halteres, whereas the seconpossesses a pair of fully functional wings. Because the thirthoracic segment acquires the identity of the second, thmutant adult fly develops a pair of wings instead ohalteres, and the transformed mutant has two pairs owings instead of one (Figure 2).

When Hox genes were discovered across a broad rangof animal phyla, many biologists began to reconsider thimportance of Richard Goldschmidts theory of saltational evolution (Jacobs, 1990; Gellon and McGinni

1998). Goldschmidts idea was that major evolutionarchanges are driven by single large-scale mutations thagenerate new morphological forms within natural populations. In this context, homeotic mutations, such as th

Figure 2 The ultrabithorax mutation, i.e. wild-type versus four-wingedfly. Provided courtesy of Sean Carroll.

Evolution of Development

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mutation in Ultrabithorax that produces a four-wingedfruitfly, appear to support Goldschimdts saltationaltheory of evolution.

However, the notion that dramatic mutations indevelopmental regulatory genes are the principal cause ofthe evolutionary transformations between animal bodyplans is incompatible with our current understanding of

neo-Darwinian theory and population genetics. Thesaltational theory in general fails to explain how suchlarge-scale homeotic mutations are fixed in naturalpopulations. The probability of a large-scale mutationbeing viable and favourably selected upon by naturalselection is very low, and should therefore have littleconsequence for evolutionary change (Fisher, 1930; Burchand Chao, 1999). It is also critical to distinguish betweenthose mutations that cause dramatic phenotypic transfor-mations in the laboratory, and those that were responsiblefor the transformations that did in fact appear and persistin natural populations over evolutionary time (Budd,1999). Furthermore, developmental regulatory genes,

including the Hox genes, play several different develop-mental roles, and can drive small-scale evolutionarychanges in a manner consistent with a gradual mode ofevolutionary change (Akam, 1998).

Stern (1998), for example, demonstrated that theUltrabithorax gene is also responsible for patterning tinybristles, called trichomes, on the second leg in D.melanogaster. He showed that evolutionary changes inthe non-protein-coding region of the Ultrabithorax geneare in part responsible for the small-scale evolutionarychanges and divergence in trichomes between closelyrelated Drosophila species. Therefore, this and Ed Lewissfour-winged fruitfly example show that changes in the non-

protein-coding regions of Hox genes can produce bothsmall-scale and large-scale mutations. For the reasonsdiscussed above, however, only the smaller-scale pheno-typic outcomes are likely to be fixed in natural populationsand contribute to the generation of morphologicaldiversity.

Hox genes provide an excellent example of howdevelopmental genes and processes can generally evolve.There are, however, many other developmental regulatorygenes that play equally important roles in the developmentand evolution of morphological structures,and which havealso been a source of conceptual advance in the field. Therole of the distal-less gene in the origin of animal

appendages (discussed below) serves as a good example.

Embryology, Palaeontology, Genes andLimbs

Evolutionary developmental biology is by nature aninterdisciplinary field, whose practitioners routinely drawupon evidence from several disciplines of biology, most

importantly genetics, embryology and morphology. Comparing data from these different biological disciplineacross taxa can reveal much about the way developmentaprocesses evolve and how they change in relation to thphenotypic features to which they give rise.

Some of the best examples of this approach come fromstudies addressing the origin of animal appendages. Th

developmental regulatory gene, distal-less, was one of thfirst genes to be examined in this context. Distal-lesprotein is a transcription factor that plays an importanrole in organizing the growth and patterning of thproximodistal axes of limbs in D. melanogaster, and iexpressed in the distal regions of the developing limb(Cohen, 1990). Thus, it came as something of a surpriswhen distal-less expression was detected in the appendages of animals from five additional phyla: (1) chordatfins and limbs, (2) polychaete annelid parapodia, (3onychophoran lobopodia, (4) ascidian ampullae, and (5echinoderm tube feet (Panganiban et al., 1997).

These results raise an interesting evolutionary question

do these similarities in gene expression indicate that thesdifferent appendages are homologous and are thereforderived from an appendage possessed by the most recencommon ancestor of these six animal phyla? Althougthere has been, and continues to be, much debatsurrounding this question, most researchers are cominto the conclusion that homology is hierarchical, and thafeatures that may be homologous at one level of biologicaorganization, such as genes and their roles, do nonecessarily indicate homology at other levels, such amorphological structures (Abouheif et al., 1997). Thpoint becomes clearer when distal-less expression examined in a historical framework, and the homolog

of different biological levels is defined independently.The fossil record of vertebrates clearly indicates that th

earliest members of this group lack limbs entirely. Thkind of historical evidence indicates that the appendages oarthropods, annelids, echinoderms and chordates, amorphological structures, are not homologous. In contrast, comparisons of sequence and expression datindicate that the distal-less gene, and possibly its role ipatterning proximodistal axes, is homologous in all othese phyla.

Thus, we have an evolutionary scenario in which nonhomologous structure is being patterned by a homologous developmental gene and by implication, a homo

logous process. This scenario can be interpreted in at leasthree ways: (1) distal-less was part of a proximodistapatterning system that patterned a limb-like outgrowth ithe ancestor of these six phyla, and was then recruited intappendage development independently in several phyla; o(2) distal-less was part of a genetic network that patterneaxes in a completely unrelated structure in the ancestor othese phyla, and was subsequently recruited independentlto pattern the proximodistal axis of nonhomologouappendages; or finally (3) the recruitment of distal-les


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into appendage development in these phyla wascompletelycoincidental, and the similarities observed in the expres-sion domains of these genes are instances of convergentevolution. It is not possible to distinguish between theseinterpretations until more comparative data becomeavailable. At the very least, however, this example hasalerted evolutionary and developmental biologists to the

possibility that the evolution of novel structures mayinvolve recruiting existing machinery for generic develop-mental tasks, such as patterning or cell signalling, ratherthan inventing them completely de novo (Shubin et al.,1997). This and other studies highlight the insights to begained from incorporating evidence from palaeontology,metazoan phylogeny, multiple taxa, and multiple levels ofbiological organization.

References

Abouheif E, Akam M, Dickinson WJ et al. (1997) Homology and

developmental genes. Trends in Genetics 13: 432433.

Akam M (1998) Hox genes, homeosis and the evolution of segmentalidentity: no need for hopeless monsters. International Journal of

Developmental Biology 42: 445451.

Budd GE (1999) Does evolution in body patterning genes drive

morphological change or vice versa? BioEssays 21: 326332.

Burch CL and Chao L (1999) Evolution by small steps and rugged

landscapes in the RNA virusf6. Genetics 151: 921927.

Cohen SM (1990) Specification of limb development in Drosophila

embryo by positional cues from segmentation genes.Nature 343: 173

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Fisher RA (1930) The Genetical Theory of Natural Selection. New Yor

Oxford University Press.

Gellon G and McGinnis W (1998) Shaping animal body plans

development and evolution by modulation of Hox expressio

patterns. BioEssays 20: 116125.

Gould SJ (1977) Ontogeny and Phylogeny. Cambridge, MA: Harvar

University Press.

Jacobs DK (1990) Selector genes and the Cambrian radiation

Bilateria. Proceedings of the National Academy of Sciences of the US87: 44064410.

Lewis EB (1978) A gene complex controlling segmentation

Drosophila. Nature 276: 565570.

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Nu sslein-Volhard C and Weischaus E (1980) Mutations affectin

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Panganiban G, Irvine SM, Sherbon B et al. (1997) The origin an

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RaffRA (1996) TheShapeof Life. Chicago: University of Chicago Pres

Shubin N, Tabin C and Carroll S (1997) Fossils, genes and the evoluti

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between Drosophila species. Nature 396: 463466.

Further Reading

Carroll SB (1995) Homeotic genes and the evolution of arthropods an

chordates. Nature 376: 479485.

Shubin N, Tabin C and Carroll S (1997) Fossils, genes and the evoluti

of animal limbs. Nature 388: 639648.


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